The Ichthyoplankton of Selected Estuaries in Sarawak and Sabah: Composition, Distribution and Habitat Affinities

Estuarine Coastal and Shelf Science (1997) 45, 197–208

The Ichthyoplankton of Selected Estuaries in Sarawak and Sabah: Composition, Distribution and Habitat Affinities S. J. M. Blabera, M. J. Farmera, D. A. Miltona, J. Pangb, O. Boon-Teckb and P. Wongb a

CSIRO Division of Fisheries, Marine Laboratories, P.O. Box 120, Cleveland, Queensland 4163, Australia Inland Fisheries Branch, Ministry of Agriculture & Community Development, Kompleks Negeri, Jl Simpang Tiga 93632, Kuching, Sarawak, Malaysia b

Received 26 March 1996 and accepted in revised form 22 July 1996 The ichthyoplankton assemblages of 23 estuaries in Sarawak and Sabah were surveyed with particular reference to the culturally and commercially important clupeid Tenualosa toli. The species composition, distribution and density of all fish larvae were recorded, together with the physical characteristics of each estuary. A more detailed study was made of the Lupar and Lassa estuaries, which are the ‘ core area ’ for T. toli. The estuaries fall into two groups. The first consists of the estuaries of the ‘ core area ’ from the Sebako in the west to the Lassa in the east, and the Labuk and Kinabatangan estuaries of eastern Sabah. They are large and deep, have middle-range salinities with no halocline, are highly turbid and have tidal ranges of >3·5 m and strong currents. There is little seasonal change in freshwater input and their waters are not peat-stained. Their total zooplankton biomasses (approximately 0·05 g m "3 dry weight, excluding fish larvae) are an order of magnitude greater than biomasses in the second group of estuaries. The second group consists of all estuaries east of the Lassa as far as the Papar in Sabah. They are mostly smaller, shallower and have more variable salinities than the ‘ core area ’ estuaries, with marked haloclines and seasonal changes in freshwater inflow, lower turbidities, weaker currents, tidal ranges of <2 m and low overall zooplankton biomasses. The composition of the ichthyoplankton is different in these two groups of estuaries. The assemblage in the first group (‘ core area ’) of estuaries consists primarily of taxa associated with estuarine and/or turbid water conditions, whereas those in the smaller estuaries of the second group have mainly marine and clearer water affinities. Only the Gobiidae are ubiquitous. Very few larvae of freshwater species were recorded in any of the estuaries. The number of fish larvae was highly variable, but the mean densities (0·01–9·23 m "3) were similar, and similarly variable, to the densities reported for other tropical estuaries. The diversity of the ichthyoplankton assemblage in Sarawak and Sabah estuaries (56 taxa, 26 families) is lower than in most other tropical estuaries of the Indo-west Pacific. This is possibly because of their rigorous physical nature, particularly the very high turbidities and current speeds, or in smaller, less physically rigorous estuaries, the low biomass of zooplankton available as food for the larvae. ? 1997 Academic Press Limited Keywords: tropical; estuaries; ichthyoplankton; habitat affinities; distribution

Introduction Although the species composition, density and seasonality of the ichthyoplankton of tropical coral reefs have been well researched (Leis & Rennis, 1983; Leis, 1991), relatively little work has been done in subtropical and tropical Indo-Pacific estuaries, apart from some work in south-east Africa (Harris & Cyrus, 1995; Harris et al., 1995), east Africa (Little et al., 1988) and Thailand (Janekarn & Boonruang, 1986). Most research on estuarine ichthyoplankton has been conducted in temperate areas (e.g. Melville-Smith & Baird, 1980; Whitfield, 1989a; Warlen & Burke, 0272–7714/97/020197+12 $25.00/0/ec960174

1990; Neira & Potter, 1992, 1994), where the habitat, zoogeographical affinities and physical conditions are very different. The clupeid Tenualosa toli (ikan terubok) is a culturally and commercially important tropical shad of the estuaries of Sarawak. In the last 10 years, it has suffered a drastic decline in numbers, so a study into all aspects of its biology and ecology was initiated in 1992 (Blaber et al., 1996). To collect information on all stages of the life cycle, including the planktonic larval stage, the species composition, distribution and density of ichthyoplankton were examined in 23 estuaries of Sarawak and Sabah, and the chief physical ? 1997 Academic Press Limited

198 S. J. M. Blaber et al. T 1. Details of the estuaries of Sarawak and Sabah included in the study together with the sampling periods, number of stations and mean dry weight of sawdust

Estuary Samunsam Sebako Santubong Sarawak Sadong Lupar Saribas Maludam Kerian Lassa Oya Mukah Balingian Kemana Suai Sibuti Baram Limbang Lawas Papar Labuk Kinabatangan Ubin

Date

Approx. river (estuary) length (km)

Number of stations

Sawdust (g m "3 &SE)

August 1994 August 1994 August 1994 August 1994 August 1994 July 1993–January 1994 August 1994 August 1994 August 1994 May 1993–January 1994 August 1994 August 1994 August 1994 August 1994 August 1994 August 1994 December 1994 December 1994 November 1994 November 1994 December 1994 December 1994 December 1994

25 (10) 15 (8) 12 (8) 35 (25) 90 (45) 130 (60) 80 (45) 20 (10) 70 (35) 100 (75) 90 (35) 50 (25) 70 (35) 70 (35) 50 (25) 40 (20) 180 (95) 90 (40) 40 (25) 50 (20) 75 (40) 100 (30) 25 (10)

4 3 2 3 5 8 1 1 2 16 3 4 2 3 5 6 2 3 7 2 3 2 3

0·001&0·0001 0·001&0·0001 0·001&0·0001 <0·001 0·105&0·105 0·088&0·066 <0·001 0·009&0·0001 0·180&0·118 0·018&0·009 0·001&0·001 <0·001 <0·001 <0·001 0·198&0·125 0·114&0·070 None None 0·162&0·058 0·018&0·004 None 0·001&0·0001 None

The estuaries are listed from west to east (see Figure 1).

characteristics of these estuaries were documented. Particular attention was given to the ‘ core estuaries ’ where T. toli are known to spawn (Blaber et al., 1996). The non-fish part of the zooplankton is described separately elsewhere (Blaber et al., 1995). The study was not intended to be exhaustive, but it is nonetheless the first large-scale survey of ichthyoplankton assemblages in Sarawak and Sabah estuaries, and serves as a basis for future research. The objectives of the present paper are: (1) to describe the ichthyoplankton of Sarawak and Sabah estuaries in relation to the physical characteristics of the estuaries, especially as regards T. toli larvae; (2) to describe the habitat affinities of the ichthyoplankton assemblages (whether marine, estuarine or freshwater species of fish); and (3) to compare the species composition and density of the ichthyoplankton with that in other tropical habitats as well as in temperate and warm temperate estuaries. Study areas The estuaries surveyed, the number of stations in each and the dates of sampling are listed in Table 1. The

locations of the estuaries are shown in Figure 1. The most detailed sampling was undertaken in the Lupar and Lassa [the core estuaries for T. toli (Blaber et al., 1996)]; enlargements of these estuaries are also shown in Figure 1.

Methods Physical characteristics During 1993, detailed surveys were made of the physical conditions in the Lupar and Lassa estuaries. Salinity, temperature, turbidity and current speed were measured in the middle reaches of the Lupar (at Lingga) and Lassa (at Teba Ang-S6) estuaries in May–June 1993 (Figure 1) and along their lengths in October 1993 (Figure 1). Plankton samples from many of the estuaries contained large amounts of sawdust, assumed to originate from sawmills along the banks in the upper reaches. Information on the (often very high) density of sawdust in the water was collected in order to investigate whether it may affect the composition or abundance of the plankton.

Ichthyoplankton in Sarawak and Sabah 199 110° E

115° Labuk

Papar Limbang Kemana Baram Lawas Balingian Suai Miri Sibuti Kerian Mukah Saribas Lassa Sabah Maludam Oya Brunei Lupar

Kinabatangan

Sadong

4° N

Sarawak

Ubin

Santubong Sebako

Sarawak

Samunsam

2°

Kalimantan 111°30' E

111° E South China Sea

South China Sea S1

Btg Lupar Mouth

Btg Lassa

Buloh Ayam Pulau Seduku

S16 S14

1°30' N S6

S12

S4

S13 2°30' N

Lingga S10

F 1. The location of estuaries sampled for ichthyoplankton in Sarawak and Sabah and details of sampling stations in the Lassa and Lupar estuaries.

In 1994, detailed information was collected on the physical characteristics of an additional 21 estuaries (Table 1) in order to help assess and explain the distribution of ichthyoplankton. The number of physical measurements made at each estuary depended on its size and length. Only the estuarine parts of the rivers were sampled. Data on the physical parameters were obtained by the following methods: Salinity. Vertical profiles from surface to bottom were measured to the nearest part per thousand with a TPS 90FL (Brisbane) Digital Salinity- Temperature-pHOxygen meter. Temperature. Vertical profiles from surface to bottom were measured to the nearest 0·1 )C with a TPS

(Brisbane) Digital Salinity-Temperature-pH- Oxygen meter. Turbidity. Surface (top 10 cm) turbidities were measured to the nearest 1 NTU (Nephelometric Turbidity Unit) with a Hach 2100P Turbidimeter. Current speeds. These were measured with an Ott ‘ propeller-type ’ current meter. Rainfall data. These were obtained from published and unpublished records of the Sarawak Department of Irrigation and Drainage for the previous 10 years (1985–94). Tidal height data. These were obtained from the 1994 official Tide Tables of the Hydrographic Directorate of the Royal Malaysian Navy.

200 S. J. M. Blaber et al.

Ichthyoplankton Fieldwork. Plankton were sampled with a square frame (50#50 cm) net of 500 ìm mesh, 3 m long. In the Lassa estuary, this was deployed passively (because of fast current speeds) from an anchored floating laboratory for either 15 or 30 min in conjunction with an Ott current meter. In all other estuaries, the net was towed from a boat at the surface at about 3 km h "1 for 10 or 15 min. In estuaries with a marked halocline (eastern Sarawak and Sabah), vertical hauls were made from bottom to surface so as to integrate samples and take account of possible differences in distributions. All plankton samples were stored in 70% ethanol for later analysis at CSIRO in Brisbane. In the T. toli ‘ core estuaries ’ of the Lupar and Lassa, plankton samples were collected in the wet and dry seasons. In the Lupar, this was in July and October 1993 (dry) and January 1994 (wet); and in the Lassa in May, July and October of 1993 (dry) and January 1994 (wet). Samples were collected from the lower, middle and upper reaches of both estuaries. In addition, to examine diel and tidal variations in the Lassa, 17 samples were collected in May 1993 over a 70-h period at the surface and 10 m depth at one station (Teba Ang) in the middle reaches; and 24 samples were collected in October 1993 from eight stations from the mouth to the ebb and flow. In all, 16 plankton samples were collected from the Lupar estuary and 54 from the Lassa estuary. At the other estuaries (Table 1), the number of samples taken per estuary varied according to conditions. Where possible, however, lower, middle and upper reaches samples were taken. A total of 69 plankton samples were collected from these 21 estuaries. Laboratory work. All the plankton samples were analysed by the following procedure: (1) Depending on the number of animals or the volume of sawdust (or both), either the entire samples were analysed or they were split (subsampled) with a Folsom Splitter. (2) Fish larvae were removed from the sample under magnification for counting and identification. They were identified to the lowest possible taxonomic level, generally family. A variety of reference sources were used to identify the larvae, including Leis and Rennis (1983) and Leis and Trnski (1989). Particular attention was paid to identifying T. toli larvae (identifiable from specimens kept from previous culture experiments). The size range of each fish taxon in each sample was recorded.

(3) Dry weights for sawdust were calculated by drying the entire sample and subtracting the total dry weight of all the animals removed from the sample. Multiple regression analyses were performed to check for any possible correlations between the occurrence and quantity of sawdust and the biomasses of (a) total zooplankton, (b) calanoid copepods and (c) fish larvae).

Results Lassa and Lupar estuaries The physical conditions at the sample sites in the middle reaches of each of these estuaries were monitored at different stages of the tide in May–June 1993. At Teba Ang in the Lassa estuary, surface salinities varied from 0 to 7 according to the state of the tide; surface temperature was a uniform 28 )C; surface turbidity, which was high, ranged from 119 NTU on the slack high tide to 627 NTU on the rising tide. Current speeds at the surface and at 10 m depth were highest during the rising tide (almost 1 m s "1) and lowest at slack tide. Conditions at Lingga in the Lupar estuary were similar: surface salinities varied from 4 to 11 with the state of the tide; surface temperature was a uniform 28 )C; and surface turbidity was high (ranging from 105 NTU on the slack tide to 664 NTU on the rising tide). Current speeds, which were measured only on the ebbing tide, approached 1 m s "1 at the surface and at 10 m depth. Measurements of physical parameters were made in October 1993 along the lengths of the Lassa and Lupar estuaries at the stations shown in Figure 1. Along the Lassa estuary, salinities fell from 22 offshore of the mouth to completely fresh about 75 km from the mouth. Uniform surface and bottom salinities at Teba Ang indicated that there was no halocline. Turbidities at the mouth were highly variable (34–163 NTU), while in the estuary, they were highest in the middle reaches (417 NTU) but fell markedly after the ebb-and-flow point (9 NTU) at the top of the estuary. Current speeds reached a maximum of 0·9 m s "1 on the rising and ebb tides. Conditions in the Lupar estuary were similar, although salinities were more uniform (9–14) along its length. Turbidities were high (38–167 NTU) but generally lower than in the Lassa estuary, except in the upper reaches where they measured over 1000 NTU in the shallow waters around Pulau Seduku. Current speeds were similar to those in the Lassa.

Ichthyoplankton in Sarawak and Sabah 201

Other estuaries of Sarawak and Sabah

40 (a)

Turbidity. Median turbidities for the mouth, middle reaches and upper reaches of each estuary are shown in Figure 3. As with salinity, the estuaries could be divided into two groups based on their turbidity regimes: (1) Estuaries with high turbidities, usually above 50 NTU. They are also very variable and have very high maximum turbidities, particularly in the middle and upper reaches where values are often above 300 NTU. This group includes those of the ‘ core area ’ for T. toli, particularly the large Sadong, Lupar and Lassa estuaries, as well as the smaller Maludam and Kerian estuaries. (2) Estuaries with relatively low turbidities and low variability. They typically have values of less than 50 NTU (usually less than 20 NTU) and include most of

Salinity

0 40 (b)

30

20

10

0 40 (c)

30

20

10

0

Samusam Sebako Santubong Sarawak Sadong Lupar Maludam Kerian Lassa Oya Mukah Balingian Kemana Suai Sibuti Baram Limbang Lawas Papar Labuk Kinabatangan Ubin

Temperature. Temperatures varied either within or between estuaries. Vertical stratification was minimal and no evidence of a thermocline was recorded in any estuary. As expected in tropical systems, the temperature range was small, from 25·8 to 31·0 )C. Variations in temperature were related primarily to time of day and weather.

20

10

Salinity

(1) Estuaries with relatively stable mid-range salinities for much of their length and with complete vertical mixing (no halocline). This group includes the large estuaries of the ‘ core area ’ (the Sadong, Lupar and Lassa) as well as the Santubong and Sebako estuaries in the west, and the large estuaries of the east coast of Sabah (the Labuk and Kinabatangan). (2) Estuaries with highly variable salinities and with a marked halocline. This discontinuity, usually at between 2 and 5 m depth, separated low-salinity water (usually less than 5) from high-salinity marine water (usually more than 25). This group includes all the estuaries east of the Lassa (the Oya, Mukah, Balingian, Kemana, Suai, Sibuti, Baram, Limbang, Lawas and Papar). In the west, it includes the Sarawak and Samunsam estuaries, which exhibit marked vertical salinity stratification.

30

Salinity

Salinity. The salinity ranges recorded in each of the estuaries are shown in Figure 2. The ranges for the Lassa and Lupar estuaries are also shown in Figure 2 for comparison. Values are plotted separately where possible for the mouth, middle reaches and lower reaches of each estuary. Although there is considerable variation within estuaries they can be divided into two main groups:

F 2. Salinity ranges in the (a) lower, (b) middle and (c) upper reaches of each estuary.

the smaller systems. All estuaries east of the Lassa fall into this group and all estuaries west of the Sarawak. Rainfall. Sarawak and Sabah receive a high annual rainfall but it is not evenly distributed throughout the

202 S. J. M. Blaber et al. 6

10 000

5 Mean tidal height (m)

100

10

3

2

Ubin

Kinabatangan

Lawas

Limbang

Baram

Bintulu

Mukah

Oya

Lassa

Lupar

Balingian

F 3. Median turbidities of the lower ( ), middle ( ) and upper reaches ( ) of each estuary.

Sarawak

0

Santubung

1

Samusam Sebako Santubong Sarawak Sadong Lupar Maludam Kerian Lassa Oya Mukah Balingian Kemana Suai Sibuti Lawas Papar Labuk Kinabatangan Ubin

1

4

Lundu

Turbidity (NTU)

1000

River

year, and it varies with location. The amount of rainfall influences river flow, and hence salinity and turbidity, and is a good indicator for the amount of freshwater entering the estuaries. Although all estuaries received rainfall in all months of the year, there appears to be a change in the pattern from west to east. In the west, more of the rain falls between November and March [10-year (1985–94) monthly means of 750 mm in December and January; 100– 200 mm in May–August] whereas further east it is more evenly distributed [10- year (1985–94) monthly means approximately 250 mm month "1] throughout the year.

Tidal heights. The tidal regime in an estuary has a marked effect on both salinity patterns and current flows. The amplitude of the tides is not the same in all the estuaries of Sarawak and Sabah. The 1994 mean high water values, together with the highest astronomical tides, are shown in Figure 4 for each estuary for which measurements are available. The estuaries fall into two groups based on tidal range: (1) Estuaries with a tidal range greater than 3·5 m, in some instances reaching 6 m. This group includes the westernmost estuaries as far east as the Lassa, and encompasses the T. toli ‘ core area ’, particularly the Lupar and Lassa estuaries. (2) Estuaries with a tidal range of about 2 m stretch from the Oya in Sarawak to the Papar in Sabah. These

F 4. Mean high water tide heights (1994) (solid bars), together with the highest astronomical tides in Sarawak estuaries.

are the estuaries in which T. toli has not been recorded (Blaber et al., 1995). Sawdust The amounts of sawdust varied considerably between estuaries and between reaches within estuaries (Table 1). This variation can probably be ascribed to differences in sampling times and locations. Nevertheless, the estuaries with high concentrations of sawdust were the Sadong, Kabong, Lassa, Suai, Sibuti and Lawas. In these estuaries, the amounts of sawdust (by weight) were usually more than twice the total of all the zooplankton. The multiple regression analyses showed that there were no significant positive or negative correlations between the occurrence and quantity of sawdust and the biomasses of (a) total zooplankton, (b) calanoid copepods and (c) fish larvae for any estuary or any combination of estuaries. In the Lassa estuary, little or no sawdust was found in the lower reaches, but levels reached one-fifth of the plankton in the middle reaches, and were 10 times greater in the upper-middle reaches (0·02 g m3 dry weight). The absence of much sawdust in the lower reaches compared with the upper reaches suggests that it may have a high residence time in the upper reaches.

Ichthyoplankton in Sarawak and Sabah 203 Lupar estuary

Lassa estuary

15.0

9.0

35.0

7.5

34.4

38.4 40.6 9.9

Clupeidae

Engraulididae

Sciaenidae

Clupeiformes

Gobiidae

Tetraodontidae

Other

F 5. The proportions by numbers of individuals of each of the main ichthyoplankton taxa in the Lupar and Lassa estuaries.

In the Lupar estuary, the amount of sawdust in the water column mirrored the situation in the Lassa, with a sharp increase in January 1994 that could not be accounted for. Ichthyoplankton General features. A total of 14 773 individuals of 56 taxa from 26 families was recorded from all estuaries during the survey, and for the Lupar and Lassa estuaries throughout the study period. The numbers of taxa recorded from the Lupar (25) and Lassa (46) were much higher than from the other estuaries, probably because of the greater number of samples taken in these ‘ core estuaries ’. The relative proportions of each of the main taxa in the Lupar and Lassa estuaries for all samples combined are shown in Figure 5. Similar numbers of gobies occurred in each but the proportion of sciaenids and tetraodontids were higher in the Lassa; the relative numbers of clupeids and engraulids are confused by the numbers of unidentifiable clupeiform larvae, but the total of all Clupeiformes (Clupeidae, Engraulididae and Clupeiformes) was higher in the Lupar estuary. The frequency of occurrence of each of the 26 families (+unidentifiable Clupeiformes) in the 23 estuaries is shown in Figure 6. Gobiidae occurred in 21 estuaries, Clupeiformes in 11, Engraulididae

in eight, Sciaenidae in six and Blenniidae in five. Another 14 families occurred in only one estuary each. The mean densities of fish larvae in the 23 estuaries are listed in Table 2. In most cases, because of the small number of samples, the standard errors of the means are high and there are few significant differences between estuaries. However, it is noteworthy that mean densities were generally much higher in the smaller estuaries east of the Lassa. In the Lupar and Lassa estuaries, where sufficient samples were taken to permit comparison, densities were significantly higher in the Lupar. Differences between sampling months in the density of larvae in the Lupar and Lassa are shown in Table 3; in both estuaries, densities were highest in September and October. Diel changes in numbers of larvae on the surface and at a depth of 10 m were plotted over a 70-h period in the middle reaches of the Lassa (Figure 7). The density of larvae did not correlate with time of day but there are indications of a tidal influence. Numbers were greatest in surface waters at low tide and in deeper waters on the high to ebbing tide. Major families Clupeidae. Tenualosa toli larvae (Terubok). These were found only in the Lassa and Lupar estuaries. They were all from the middle and upper reaches and their

Taxa

204 S. J. M. Blaber et al. T 2. Overall mean density of ichthyoplankton in each estuary (listed from west to east) and total numbers of individual larvae (n) in samples

Trichiuridae Siganidae Pangasiidae Ostraciidae Mugilidae Lutjanidae Hemiramphidae Harpadontidae Eleotridae Carangidae Atherinidae Apolectidae Ambassidae Triglidae Synodontidae Cynoglossidae Clupeidae Ariidae Tetraodontidae Apogonidae Syngnathidae Polynemidae Blenniidae Sciaenidae Engraulididae Clupeiformes Gobiidae

Estuary

0

10 20 Number of estuaries

F 6. The frequency of occurrence of 26 families (+Clupeiformes) of ichthyoplankton in 23 estuaries of Sarawak and Sabah.

size (14–37 mm; May–November) suggested that they had been spawned in the estuary. Their absence from other estuaries, together with information on the reproductive condition of this fish from throughout Sarawak (Blaber et al., 1996), indicates that the Lupar and Lassa estuaries might be the only spawning grounds. In marked contrast to the abundance of gobiid, Coilia and sciaenid larvae, the numbers of T. toli larvae were low (a total of 50). This probably reflects the endangered status of Terubok and the low numbers of adults. Very small (<10 mm) clupeid larvae that could not be identified to genus, but that might be T. toli, were recorded in the Lupar and Lassa but in no other estuaries. Other unidentified clupeiform larvae were present in 11 estuaries. Gobiidae. This family was recorded in almost all estuaries. Most specimens were too small to be identified (0·4–20 mm) but the following genera were recorded: Apocryptodon (11 mm), Gobiopterus (6– 10 mm), Pandaka (6–9 mm) and Periophthalmus (8– 9 mm). Numbers were highest in the eastern estuaries: 11·6 m "3 in the Baram, 10·6 m "3 in the Sibuti, 9·9 m "3 in the Limbang and 5·8 m "3 in

Samunsam Sebako Santubong Sarawak Sadong Lupar Saribas Maludam Kerian Lassa Oya Mukah Balingian Kemana Suai Sibuti Baram Limbang Lawas Papar Labuk Kinabatangan Ubin Total

Mean n m "3 &SE 0·036&0·016 0·028&0·01 0·167&0·153 0·029&0·006 0·251&0·086 0·285&0·083 1·113&1·097 0·340&0·107 0·284&0·242 0·132&0·024 0·280&0·116 0·027&0·013 0·360&0·193 0·080&0·023 4·150&2·420 9·230&3·132 7·917&3·954 6·586&4·301 3·813&1·518 0·010& <0·001 0·561&0·205 0·028&0·011 0·097&0·063

n 16 17 50 13 565 4167 835 68 284 7196 126 19 108 48 189 85 95 169 61 2 617 14 29 14 773

the Suai; and lowest in the western estuaries from Samunsam to Oya (0·01–0·49 m "3) and in Sabah estuaries (0·01–0·87 m "3). Engraulididae. Five genera were recorded: Coilia, Lycothrissa, Setipinna, Stolephorus and Thryssa. Six species of Coilia were collected, mainly from the Lupar and Lassa estuaries. They were one of the most abundant groups of fish larvae and juveniles in the plankton from the Terubok ‘ core area ’; their T 3. Mean densities (n m "3 &SE) of ichthyoplankton in the Lupar and Lassa estuaries during 1993 and 1994 Month and year

Lupar estuary

Lassa estuary

May 1993 June 1993 August 1993 September 1993 October 1993 November 1993 January 1994 August 1994

– 0·27&0·25 0·09&0·05 0·37&0·17 0·67&0·39 – 0·16&0·09 0·27&0·26

0·04&0·01 – – 0·41&0·18 0·28&0·07 0·08&0·03 0·09&0·05 –

–, no sample.

Ichthyoplankton in Sarawak and Sabah 205

Low 0.7

High

Tide level Low High

Low

tide

Numbers of larvae (m–3)

0.6

Polynemidae. Threadfin larvae were recorded from the Lassa, Maludam and Kabong estuaries in August and October (0·018–0·496 m "3; 7–37 mm). Tetraodontidae. Chonerhinos modestus occurred in the ‘ core estuaries ’ of the Lupar, Sadong and Lassa (0·07–0·23 m "3; 2–39 mm), while C. remotus was found only in the Lassa (0·04 m "3; 6–15 mm). Unidentifiable tetraodontid larvae were also found in the Lassa and Lupar estuaries, but nowhere else.

0.5 0.4 0.3

Syngnathidae. Unidentified pipefish larvae were found in the Sadong, Lupar, Lassa and Saribas estuaries (0·007–0·012 m "3; 17–29 mm).

0.2 0.1

1200

Minor families 1200

1200

0.0

Time of day (h)

F 7. Diel changes over 70 h in the numbers of fish larvae on the surface ( ) and at 10 m depth ( ) in the middle reaches of the Lassa estuary in May 1993.

densities ranged from 0·003 to 1·37 larvae m "3. This genus was recorded only once (in Balingian) outside the Terubok ‘ core area ’. Small larvae that could not be assigned to a species were classified as Coilia spp. These larvae peaked in abundance in June, but were present in all sampling months. The overall length range of all Coilia, including juveniles, caught in the plankton was 4–109 mm. The larvae of three species of Setipinna (S. breviceps, S. taty and S. tenuifilis) were recorded in the middle and upper reaches of the Lassa between May and October (densities of 0·002–0·01 m "3; lengths of 22–28 mm). Lycothrissa was found only in the Lassa (0·005 m "3; 23 mm), juveniles of Stolephorus baganensis were found in both the Lupar and Lassa (0·007 m "3 in both systems; 39–44 mm) and Thryssa baelama were found in the Lupar and Maludam estuaries (0·007–0·38 m "3; 13–25 mm). Sciaenidae. Sciaenids were one of the most abundant groups of fish larvae but were also confined mainly to the estuaries of the T. toli ‘ core area ’. The family is large, with many species occurring in Sarawak. Unfortunately, it was not possible to separate the species in the study. They were present throughout the year but were most numerous between August and October with densities reaching 0·38 larvae m "3. In the Lassa estuary in October 1993, they were most abundant in the middle reaches. The overall length range recorded was 2–23 mm.

Seventeen other families that were not well represented in the samples (Ambassidae, Apogonidae, Apolectidae, Atherinidae, Blenniidae, Cynoglossidae, Eleotridae, Harpodontidae, Hemiramphidae, Lutjanidae, Mugilidae, Ostraciidae, Pangasiidae, Siganidae, Synodontidae, Trichiuridae and Triglidae) comprised only 208 individuals, about half of which were Blenniidae. Many were represented only by one or two individuals. Discussion The estuaries of Sarawak and Sabah fall into two well-defined groups based on their physical characteristics (Table 4). The first group consists of the estuaries of the T. toli ‘ core area ’, from the Sebako in the west to the Lassa in the east, as well as the Labuk and Kinabatangan estuaries of eastern Sabah. These systems are large and deep. They have middle-range salinities with no halocline, high turbidity, tidal ranges of >3·5 m and strong currents. There is little seasonal change in freshwater input (rainfall more evenly distributed) and their waters are not peat-stained. In addition, their total zooplankton biomasses (about 0·05 g m "3 dry weight, excluding fish larvae), consisting mainly of calanoid copepods, are an order of magnitude greater than biomasses in the second group of estuaries (Blaber et al., 1995). The second group consists of all the estuaries east of the Lassa as far as the Papar in Sabah. They are mostly smaller, shallower and have more variable salinities with a marked halocline, marked seasonal changes in freshwater inflow, lower turbidities, weaker currents, tidal ranges of <2 m and usually low zooplankton biomassses. The distribution of ichthyoplankton is apparently strongly related to these two groups of estuaries. The following taxa were found almost solely in the first

206 S. J. M. Blaber et al. T 4. Comparison of the main features of the two groups of estuaries in Sarawak and Sabah Feature

Group 1 Characteristics

Group 2 characteristics

Size Salinity

Large and deep (>10 m) Mid-range in middle reaches Long-term stability Full vertical mixing High, usually >50 NTU Evenly distributed throughout the year Tidal range >3·5 m Current speeds to >1 m s "1 High overall biomass Calanoid copepods are >60% of biomass Water not peat-stained

Usually smaller 0–30 Highly variable Marked halocline Low, seldom >20 NTU Peaks from November to March Tidal range 2 m or less Current speeds usually <1 m s "1 Variable, usually low biomass Low biomass or no calanoid copepods Water usually peat-stained with low pH

Turbidity Freshwater (rainfall) inflow Tides Zooplankton (Blaber et al., 1995) Other NTU, nephelometric turbidity unit.

group of larger estuaries: Chonerhinos spp., Clupeidae (including T. toli), Coilia spp., Cynoglossidae, Eleotridae, Polynemidae, Sciaenidae, Setipinna spp., Stolephorus spp., Thryssa spp. and Lycothrissa sp. Four taxa, Syngnathidae, Apogonidae, Blenniidae and Siganus spp., were more or less restricted to the smaller estuaries of the second group. Only the Gobiidae were ubiquitous, and they were an important component of the assemblage in almost all estuaries. Gobies are a large component of fish larval assemblages in many estuarine and marine areas throughout the world: temperate South African and West Australian estuaries (Beckley, 1986; Neira et al., 1992), subtropical African estuaries (Harris & Cyrus, 1995; Harris et al., 1995), temperate surf zones (Whitfield, 1989a), tropical mangroves (Janekarn & Boonruang, 1986; Little et al., 1988), tropical nearshore waters (Janekarn & Kiørboe, 1991a) and tropical continental shelves (Young et al., 1986). This widespread occurrence of gobiid larvae in large numbers is probably a result of the very large numbers of species in this, the largest family of marine fishes (Nelson, 1984), especially in the tropics, and the relatively long duration of their larval phase (Thresher, 1984). The ichthyoplankton in the first group of estuaries were primarily from taxa whose adults were found in estuarine or turbid water, whereas those in the smaller estuaries of the second group are found mainly in marine and clearer waters (Blaber & Blaber, 1980; Blaber, 1981; Cyrus & Blaber, 1992). Some in the first group such as T. toli (Blaber et al., 1996) and Coilia spawn in the estuaries, while others, such as Sciaenidae and Polynemidae, spawn both in the lower reaches of the estuaries and in adjacent shallow coastal waters. There is no clear cut-off point between the large estuaries and the shallow coastal waters in terms

of salinity or turbidity (Blaber, 1981). However, the fish fauna in these waters is different from that of the offshore shelf (Latiff et al., 1976), with few species in common. As the larvae of only two freshwater genera (Chonerhinos and Pangasius) were recorded in this study, it is probable that few of the larvae of the large and diverse freshwater fish fauna of Borneo (Roberts, 1989; Inger & Chin, 1990) penetrate estuaries. The relatively low number of T. toli larvae recorded in the estuaries in which the adults spawn is probably an indication of the small population of this species. It is noteworthy in this context that experimental work on the eggs and larvae of North American alosids found that high concentrations of suspended sediment significantly reduced the survival rate of larvae (Auld & Schubel, 1978). Unfortunately, there are no data on the turbidity of the Lupar or Lassa estuaries before agriculture and forestry developed in the catchment, and it is not known whether the sediment loads have increased in recent years. The number of fish larvae in Sarawak and Sabah estuaries is highly variable, but the mean densities (0·01–9·23 m "3) are similar, and similarly variable, to the densities recorded for other tropical estuaries: 0·01–0·52 m "3 in the Kosi estuary of northern Natal (Harris et al., 1995), 0·15–10·3 m "3 in the St Lucia system of Natal (Harris & Cyrus, 1995), 1·2–2·0 m "3 in an East African mangrove creek (Little et al., 1988) and 0·04–0·20 m "3 in Thailand (Janekarn & Kiørboe, 1991a). In southern hemisphere temperate estuaries, similar densities have been recorded: 3·9 m "3 in the Swartkops estuary in South Africa (Beckley, 1985), 0·22–0·47 m "3 in the Swartvlei estuary in South Africa (Whitfield, 1989b) and 0·04– 3·14 m "3 in the Swan estuary in Western Australia (Neira et al., 1992). In tropical, non-estuarine areas, values are also similar. In the Andaman Sea off

Ichthyoplankton in Sarawak and Sabah 207

western Thailand, mean densities were generally >0·1 m "3 away from shore and <0·1 m "3 nearshore, with overall coastal densities of 1·5–1·9 m "3 (Janekarn & Kiørboe, 1991b). The mean density in the Arabian Gulf was 3·89 m "3 (2·8–10·3 m "3) (Houde et al., 1986), while on the north-west Shelf of Australia, mean densities were lower (0·01– 0·04 m "3) (Young et al., 1986). In a large-scale study of Thai coastal ichthyoplankton, Janekarn and Kiørboe (1991b) found that larval density was negatively correlated with turbidity. In Sarawak and Sabah, the mean density of ichthyoplankton was higher in most of the small, clearer water estuaries east of the Lassa than in the larger, more turbid estuaries of the T. toli ‘ core area ’. However, Gobiidae contributed most of the numbers in the smaller estuaries and diversity was low. The diversity of ichthyoplankton in Sarawak and Sabah estuaries (56 taxa, 26 families) is lower than that reported for other tropical estuaries of the Indowest Pacific, with the exception of a mangrove creek in Kenya (at least 25 families; Little et al., 1988). In Thailand, 44 families were recorded (Janekarn & Boonruang, 1986); in the Kosi and St Lucia estuaries (both in Natal) 61 families (153 taxa) and 44 families (85 taxa) were recorded (Harris & Cyrus, 1995; Harris et al., 1995); in the tropical shelf waters of north-west Australia, 104 taxa were recorded (Young et al., 1986); and in the Arabian Gulf, 84 taxa were recorded (Houde et al., 1986). Even the temperate waters of the Swan estuary in West Australia contained 74 species (Neira et al., 1992). Seasonal abundance data are not available from the present study for most of the estuaries of Sarawak and Sabah, most samples being taken during the dry (less wet) season, so the diversity may in fact be higher. However, in the Andaman Sea, densities and diversities were highest during the dry season (Janekarn & Kiørboe, 1991b). On the other hand, the relatively low diversity may be real. It is possibly the result of the very high turbidities and current speeds in the larger estuaries, or the low biomass of zooplankton available as food for the larvae (Blaber, et al., 1995) in the smaller, less physically rigorous, estuaries. Acknowledgements This project was funded by the Ministry of Agriculture and Community Development, Sarawak Government and PPES Aqua (Santubong) Sdn Bhd (SEDC). The project participants are very grateful to Datuk Amar Alfred Jabu anak Numpang for his interest and support; to Leonard Martin Uning, Henry Jantum and Hang Tuah Merawin for their support; and to

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